Genetic differentiation and inferred dynamics of a hybrid zone between Northern Spotted Owls (Strix occidentalis caurina) and California Spotted Owls (S. o. occidentalis) in northern California

Abstract

Genetic differentiation among Spotted Owl (Strix occidentalis) subspecies has been established in prior studies. These investigations also provided evidence for introgression and hybridization among taxa but were limited by a lack of samples from geographic regions where subspecies came into close contact. We analyzed new sets of samples from Northern Spotted Owls (NSO: S. o. caurina) and California Spotted Owls (CSO: S. o. occidentalis) in northern California using mitochondrial DNA sequences (mtDNA) and 10 nuclear microsatellite loci to obtain a clearer depiction of genetic differentiation and hybridization in the region. Our analyses revealed that a NSO population close to the northern edge of the CSO range in northern California (the NSO Contact Zone population) is highly differentiated relative to other NSO populations throughout the remainder of their range. Phylogenetic analyses identified a unique lineage of mtDNA in the NSO Contact Zone, and Bayesian clustering analyses of the microsatellite data identified the Contact Zone as a third distinct population that is differentiated from CSO and NSO found in the remainder of the subspecies' range. Hybridization between NSO and CSO was readily detected in the NSO Contact Zone, with over 50% of individuals showing evidence of hybrid ancestry. Hybridization was also identified among 14% of CSO samples, which were dispersed across the subspecies' range in the Sierra Nevada Mountains. The asymmetry of hybridization suggested that the hybrid zone may be dynamic and moving. Although evidence of hybridization existed, we identified no F1 generation hybrid individuals. We instead found evidence for F2 or backcrossed individuals among our samples. The absence of F1 hybrids may indicate that (1) our 10 microsatellites were unable to distinguish hybrid types, (2) primary interactions between subspecies are occurring elsewhere on the landscape, or (3) dispersal between the subspecies' ranges is reduced relative to historical levels, potentially as a consequence of recent regional fires.

Whole-genome sequences suggest long term declines of spotted owl (Strix occidentalis) (Aves: Strigiformes: Strigidae) populations in California

“…We found higher nucleotide diversity in the Nevada County Strix occidentalis occidentalis population than in the Humboldt County S. o. caurina population. This contrasts with the findings of prior researchers, who have reported higher nucleotide diversity in Humboldt County S. o. caurina than in Sierra Nevada S. o. occidentalis(Barrowclough et al 140 1999;Miller et al 2017), althoughBarrowclough et al (2005) found higher diversity in Lassen County than in both Humboldt County S. o. caurina and El Dorado County S. o. occidentalis. El Dorado County is approximately 90 km southeast of the location of our Nevada County sample.…”

“…We utilized whole genome sequencing data generated by a previous study (Hanna et al 2017c Miller et al (2017).…”

“…Most of these relied on mitochondrial DNA (Barrowclough et al 1999(Barrowclough et al , 2005(Barrowclough et al , 2011Haig et al 2004), which comprises a single genetic locus that does not always accurately represent the history of the entire nuclear genome. Additional studies analyzed microsatellites (Funk et al 2008), RAPD markers (Haig et al 2001), or a combination of mitochondrial DNA and microsatellites (Miller et al 2017), but these mostly focused on S. o. 55…”

Isolation by distance versus landscape resistance: Understanding dominant patterns of genetic structure in Northern Spotted Owls (Strix occidentalis caurina)

“…We analyzed a data set comprised of 10 nuclear microsatellite loci [ 11 , 15 ] that were genotyped in 339 Northern Spotted Owls sampled from throughout the majority of the subspecies’ range since the mid-1990’s ( Fig 1 ). Of the 339 individuals examined, 304 were based on data from non-hybrid individuals produced by Funk et al [ 11 ],.…”

“…Previous assessments of landscape genetics patterns in Northern Spotted Owls [ 11 ] primarily relied on the “Genetic Landscape Shape” procedure [ 12 ] in the program Alleles in Space [ 13 ], which provided a qualitative graphical depiction of landscape-scale spatial genetic structure patterns. Analyses using GENELAND [ 14 ] suggested that there were no spatial genetic clusters across the landscape [ 11 ], although Miller et al [ 15 ] later identified a small population in the southern part of the owl’s range that forms a distinct genetic cluster, possesses a unique mtDNA lineage, and has a high proportion of hybrids between Northern Spotted Owls and California Spotted Owls. In this study, we applied more refined and explicit statistical tests that evaluated associations between genetic structure patterns and landscape-level connectivity as quantified by patterns of isolation by distance and isolation by resistance.…”